Guidelines and Standards for Performance of Fetal Echocardiography
AMERICAN SOCIETY OF ECHOCARDIOGRAPHY REPORT American Society of Echocardiography Guidelines and Standards for Performance of the Fetal Echocardiogram A statement of the Pediatric Council of the American Society of Echocardiography represented by, Jack Rychik, MD, Nancy Ayres, MD, Bettina Cuneo, MD, Nina Gotteiner, MD, Lisa Hornberger, MD, Philip J. Spevak, MD, and Mary Van Der Veld, MD studies suggest improved physiological state afterINTRODUCTION birth and improved surgical outcome for infantsFetal echocardiography is the ultrasonic evaluation who have had prenatal diagnosis via fetal echocar- diography.2,3 In addition, accurate diagnosis via fetalof the human fetal cardiovascular system. General echocardiography allows for appropriate counselingantepartum obstetrical ultrasound has become a to take place and for parents to take the opportunitystandard part of gestational care and is commonly to learn about the cardiac anomaly. This knowledgeused for the determination of fetal age, size, gender, can allay parental fears, improve psychological state,or well-being and for the detection of congenital and bolster coping skills in dealing with the birth ofanomalies. A variety of maternal or fetal disorders a child with life-threatening cardiovascular illness.4may result in abnormality of the fetal cardiovascular Fetal echocardiography can also contribute tosystem to a degree which demands evaluation at a improved understanding when applied to cardiovas-level above and beyond that attainable with standard cular abnormalities unrelated to congenital heartantepartum obstetrical ultrasound. In these circum- disease. Such data, when presented in a multidisci-stances, a fetal echocardiogram should be per- plinary format, can help elucidate the pathophysiol-formed. ogy of a variety of disorders and can be used to both Improved operator skill amongst physicians per- guide and monitor disease therapy.forming general antepartum obstetrical ultrasound, Performance and interpretation of fetal echocar-in combination with increased sensitivity of presentday ultrasound systems, has resulted in improved diography requires a unique set of advanced skillsdetection of fetal cardiovascular abnormalities and and knowledge. The fetal heart is of small size andincreased requirements for more detailed evalua- dynamic in nature. A myriad of complex anatomicaltion. Congenital heart disease is the most common and physiological derangements are possible. Thecongenital anomaly found in the human.1 As the American Institute of Ultrasound in Medicine5 anddetection rates for congenital anomalies continue to the American College of Radiology6 have recom-increase, the demand for fetal echocardiography has mended performance of a 4-chamber view of thegrown. Accurate diagnosis of congenital heart dis- heart as part of the standard for an antepartumease via fetal echocardiography provides many ben- obstetrical ultrasound. However, studies haveefits. It allows for a smooth transition between the shown that when using the 4-chamber view alone,pre- and post-natal states, with the opportunity to important congenital heart disease may go unrecog-provide immediate care at birth, thereby avoiding nized.7 Addition of right and left ventricular outflowthe onset of hemodynamic compromise. Recent tract and great artery visualization improves the yield allowing for more effective screening for con-From The Children’s Hospital of Philadelphia (J.R.), Texas Chil- genital heart disease,8-10 however many anomaliesdren’s Hospital, Houston (N.A.), Hope Children’s Hospital, Oak can still be missed. Hence general antenatal obstet-Lawn, Ill (B.C.), Children’s Memorial Hospital, Chicago (N.G.), rical ultrasound can function as a screen for fetalUniversity of California San Francisco (L.H.), Johns Hopkins cardiovascular disorders; suspicion or detection of aMedical Center, Baltimore (P.J.S.), and Mott Children’s Hospital,Ann Arbor, Mich (M.V.). fetal cardiovascular abnormality requires referral forAddress reprint requests to the American Society of Echocardiog- a more comprehensive evaluation to a physicianraphy, 1500 Sunday Drive, Suite 102, Raleigh, NC 27607 (919) with expertise in fetal echocardiography. Well-787-5574. trained pediatric cardiologists, maternal-fetal medi-J Am Soc Echocardiogr 2004;17:803-10. cine specialists, or obstetrical radiologists who have0894-7317/$30.00 acquired the appropriate knowledge base and skillsCopyright 2004 American Society of Echocardiography, Property as outlined below may perform fetal echocardiogra-of ASE. Reprint of these documents, beyond single use, is prohib- phy.ited without the prior written authorization of the ASE. The purpose of this statement from the Americandoi:10.1016/j.echo.2004.04.011 Society of Echocardiography is to define the distin- 803
Journal of the American Society of Echocardiography804 Pediatric Council of the American Society of Echocardiography July 2004guishing elements of the fetal echocardiogram from Table 1 Examples of indications for fetalother forms of ultrasonic evaluation and to provide echocardiographyguidelines and standards for physician performance Maternal indications Fetal indicationsand interpretation of fetal echocardiography. ● Family history of CHD ● Abnormal obstetrical ultrasound screen ● Metabolic disorders (eg, ● Extracardiac abnormality diabetes, PKU)SKILLS AND KNOWLEDGE REQUIRED ● Exposure to teratogens ● Chromosomal abnormality ● Exposure to prostaglandin ● ArrhythmiaPerformance and interpretation of fetal echocardi- synthetase inhibitors (eg,ography requires a special set of skills and knowl- ibuprofen, salicylic acid,edge. The physician performing and interpreting indomethacin)fetal echocardiography must: ● Rubella infection ● Hydrops ● Autoimmune disease (eg, ● Increased first trimester nuchal ● be able to recognize the full spectrum of simple SLE, Sjogren’s) ¨ translucency and complex, acquired and congenital, heart ● Familial inherited disorders ● Multiple gestation and suspicion disease and its manifestations and natural his- (Ellisvan Creveld, Marfan, of twin-twin transfusion tory throughout gestation, and recognize the Noonan’s, etc) syndrome limitations of fetal echocardiography in detect- ● In vitro fertilization ing important associated lesions CHD, Congenital heart disease; PKU, phenyl ketonuria; SLE, sytemic lupus ● have the skill and ability to apply all modalities erythematosus. of echocardiography including 2-dimensional, M-mode, pulsed-wave, continuous wave, and Doppler color flow mapping in recognizing and ography will also offer counseling to the family of evaluating both the normal and abnormal fetal the fetus. In these circumstances, the physician cardiovascular state offering counsel must have a thorough knowledge ● have knowledge of the anatomy and physiology base of all management strategies and be familiar of the cardiovascular system throughout the with current outcomes for treatment of congenital stages of human development and acquired cardiovascular disease. ● have a thorough understanding of the spectrum of fetal arrhythmias and the ability to utilize the spectrum of echocardiographic modalities for INDICATIONS their assessment ● be knowledgeable in the principles of biological Indications for fetal echocardiography can be sepa- ultrasound instrumentation and its application rated into maternal and fetal indications. Examples in human pregnancy ● are listed in Table 1. have a thorough understanding of maternal-fetal There are presently no strong prenatal markers physiology as well as maternal conditions that available for identifying the fetus with congenital may affect the developing fetus ● heart disease. Family history of congenital heart be familiar with the latest developments in disease or the presence of a chromosomal anomaly obstetrical diagnostics, which include invasive are relative risk factors. Increased nuchal translu- and non-invasive tests available throughout cency present at 10 to 13 weeks gestation has been pregnancy ● associated with an increased risk of congenital heart have knowledge of the growing field of invasive disease, even in the absence of chromosomal anom- fetal intervention and its possible effects on the aly.12 Recent reports indicate up to a 3-fold increase fetal cardiovascular system. in the prevalence of congenital heart disease over Specific training requirements and maintenance the general population in infants conceived viaof competency guidelines have been developed by intracytoplasmic sperm injection and in-vitro fertili-the American College of Cardiology in conjunction zation.13with the American Heart Association and AmericanSociety of Echocardiography and are endorsed byour group.11 THE FETAL ECHOCARDIOGRAM The physician performing and interpreting fetalechocardiography should have access to a multidis- Timing of Examinationciplinary team with expertise in maternal-fetal med-icine, genetics, neonatology, pediatric surgery, pedi- The optimal timing for performance of a compre-atric cardiology, and pediatric cardiac surgery, with hensive transabdominal fetal echocardiogram is 18availability for consultative services and advice. Of- to 22 weeks gestation. Images can be more difficulttentimes the physician performing fetal echocardi- to obtain after 30 weeks gestation, as the ratio of
Journal of the American Society of EchocardiographyVolume 17 Number 7 Pediatric Council of the American Society of Echocardiography 805fetal body mass-to-amniotic fluid increases. Acquir- Table 2 Essential components of the fetaling images of the fetal heart at 15 to 18 weeks is echocardiogrampossible; however performing a comprehensive car- Feature Essential componentdiac evaluation study at this age can be difficult and Anatomic overview Fetal number and position in themay require repeat assessment at 18 to 22 weeks. uterus Establish stomach position andEquipment abdominal situsUltrasound systems used for fetal echocardiography Establish cardiac positionshould have capabilities for performing 2-dimen- Biometric examination Cardiothoracic ratio Biparietal diametersional, M-mode, and Doppler imaging. The require- Femur lengthments of fetal echocardiography are more stringent Cardiac imaging Four-chamber viewthan for the examination of an infant or child with views/sweeps Four-chamber view angledcongenital or acquired heart disease. This is due to towards great arteriesthe increased demands for both spatial and temporal (“Five-chamber” view)resolution. Anatomic surveys require axial resolu- Long-axis view (left ventriculartion of 1 mm or less and this is particularly important outflow)given the small size of critical fetal cardiac struc- Long-axis view (right ventriculartures. Frames rates of 80 to 100 Hz are frequently outflow)needed to view important events occurring at heart Short-axis sweep (cephalad angling includes “3-vessel” viewrates in excess of 140 beats per minute. To meet Caval long-axis viewthese requirements, imaging systems need to be Ductal arch viewoptimally configured. In general, system settings are Aortic arch viewadjusted to minimize persistence and spatial averag- Doppler examination Inferior and superior vena cavaing and to increase frame rate. All modalities of Pulmonary veinsDoppler including color, pulse, high pulse repeti- Hepatic veinstion frequency, and continuous wave should be Ductus venosusavailable. Tissue Doppler imaging has been recently Foramen ovaleapplied in the assessment of fetal arrhythmia.14 Atrioventricular valvesHarmonic imaging is useful when acoustic penetra- Semilunar valves Ductus arteriosustion is difficult such as in the presence of maternal Transverse aortic archobesity. Phased array transducers with fundamental Umbilical arteryfrequencies between 4 and 12 MHz are generally Umbilical veinused. Curvilinear probes may be helpful given the Measurement data Atrioventricular valve diameterwider near-field of view. High frequency transducers Semilunar valve diameterwith a narrower footprint commonly used in echo- Main pulmonary arterycardiography of infants may also be helpful. Ascending aorta Branch pulmonary arteriesExamination Technique Transverse aortic arch Ventricular lengthThe essential components of the fetal echocardio- Ventricular short-axis dimensionsgram are listed in Table 2. Although the goal is to Examination of M-mode of atrial and ventricularachieve visualization of each of the essential compo- rhythm and rate wall motionnents, not all will be visualized in every fetus at Doppler examination of atrial andevery examination. Fetal position in the uterus or ventricular flow patternsincreased activity may limit the ability to obtainvisualization of each of the components. The number of vessels in the umbilical cord is views are described below with a brief explanationcounted and Doppler sampling of the umbilical of how to achieve the view and the structuresartery and umbilical vein is performed. After estab- generally well seen. Reference sources are available,lishing the position of the fetus and the right/left and which illustrate these views in detail.15 Figures 1 andanterior/posterior orientation, an initial survey of 2 demonstrate the anatomical correlates to the to-the fetus is used to estimate the gestational age and mographic imaging planes used for the views de-to establish abdominal situs and cardiac position. scribed below. The authors recognize that based onThe presence or absence of fluid in the pericardial, operator style, alternative or additional sweeps andpleural, or peritoneal space should be noted. The views may be utilized to image the various struc-position of the inferior vena cava and descending tures of the fetal heart and still accomplish a com-aorta at the level of the diaphragm are established. prehensive fetal echocardiogram. Multiple scanning positions and sweeps are nec- Four-chamber view. The 4-chamber view is gen-essary to adequately image the fetal heart. Suggested erally easy to achieve and is useful for identifying the
Journal of the American Society of Echocardiography806 Pediatric Council of the American Society of Echocardiography July 2004 Figure 1 Illustration of the tomographic planes used to image the fetal cardiovascular system. Imaging planes displayed are in a normal human fetus. Starting at the top left, the following views are demonstrated in a clockwise manner: 1, apical (4-chamber) view; 2, apical (5-chamber) view angled towards the aorta; 3, long-axis view of the left ventricular outflow tract; 4, long-axis view of the right ventricular outflow tract; 5, short-axis view at the level of the great vessels; 6, short-axis view with caudaud angling at the level of the ventricles; 7, caval long-axis view; 8, ductal arch view; 9, aortic arch view.atria, ventricles, and respective septae (Table 3). times, the pulmonary veins can be identified enter-The diameters of the mitral and tricuspid valve ing the left atrium posteriorly.annuli are measured. The lengths of the left and Short-axis view. The short-axis view is obtainedright ventricle can also be measured. Numerous by scanning perpendicular to the long axis of thestandards for dimensional measures based on gesta- heart (Table 4). It is an excellent view for identifyingtional age have been published.16-19 The view is the return of the pulmonary veins. In general, theinadequate for determining the conotruncus and in connections of both lower lobe veins can be visual-particular, excluding transposition of the great arter- ized. The upper pulmonary veins may be identifiedies. From the standard 4-chamber view, one should as they course directly beneath the branch pulmo-sweep posteriorly to demonstrate the coronary si- nary arteries. Sweeping cranially, one can measurenus and then anteriorly to identify the aorta. Often- right ventricular and left ventricular diastolic dimen-
Journal of the American Society of EchocardiographyVolume 17 Number 7 Pediatric Council of the American Society of Echocardiography 807 Figure 2 Illustrations of the anatomical correlates for each of the designated tomographic imaging planes used for imaging of the fetal cardiovascular system. Each numbered view relates to the clockwise illustration of the fetal heart in Figure 1. Ao, Aorta; IVC, inferior vena cava; LA, left atrium; LV, left ventricle; MV, mitral valve; PA, pulmonary artery; PD, patent ductus; RA, right atrium; RV, right ventricle; SVC, superior vena cava.
Journal of the American Society of Echocardiography808 Pediatric Council of the American Society of Echocardiography July 2004Table 3 Structures viewed in the 4- and 5- chamber view Table 5 Structures viewed in the cardiac long-axis sweep● Atrial and ventricular size ● Superior and inferior vena cava● Atrial and ventricular septae ● Left ventricular outflow tract● Atrioventricular size and function ● Ascending aorta● Coronary sinus ● Great vessel connection and size● Ventricular function in long axis ● Ductus arteriosus and proximal ductal arch● Semilunar valve function (may not, however, be optimal to differentiate aorta from main pulmonary artery)● Pulmonary veins Table 6 Structures viewed in the caval long-axis view ● Superior vena cava ● Inferior vena cava and eustachian valveTable 4 Structures viewed in the cardiac short-axis sweep ● Patent foramen ovale● Pulmonary venous return ● Right pulmonary artery● Inferior vena cava and hepatic veins● Ventricular short-axis dimensions● Ventricular-arterial relationship Table 7 Structures viewed in the ductal and aortic arch● Right ventricular outflow tract views● Branch pulmonary arteries and origin● Caval connections ● Main pulmonary artery● Innominate vein ● Branch pulmonary arteries● Ductus arteriosus ● Patent ductus arteriosus and direction of flow● Determination of arch sidedness and branching ● Aortic arch dimension (ascending, transverse, isthmus, and descending) ● Direction of flow in the aortic archsions. These measurements should be made at thelevel of the tips of the papillary muscles of the leftventricle. Even more cranially, one can identify the ing to the right allows visualization of both cavaemain pulmonary artery as it supplies the branch (although these structures are better visualized inpulmonary arteries. Identification of the branch the caval view described below).pulmonary arteries facilitates determination of the Caval long-axis view. The caval long-axis view isconotruncus. The superior vena cava can be identi- obtained with the imaging plane parallel to the cavalfied crossing anterior to the ipsilateral branch pul- connections to the right atrium (Table 6). Continuitymonary artery. Even more superiorly, the innomi- of the inferior vena cava as it passes through thenate vein is noted and as well, the branching of the liver is established. The septum primum is seenaortic arch and arch sidedness. Sweeping inferiorly extending into the left atrium. Color Doppler inter-one can demonstrate the connection of the inferior rogation demonstrates the normal right to left flowvena cava and hepatic veins with the right atrium. A across the foramen ovale, which is reversed incross-sectional view obtained at the level of the lesions of critical left heart hypoplasia.20superior mediastinum provides an image of the Ductal view and aortic arch view. The ductal view“3-vessel view.” In this plane the relationship and is obtained when the imaging plane is aligned withsize differences between the superior vena cava, the the right ventricular outflow tract and main pulmo-ascending aorta, and main pulmonary artery can be nary artery. The aortic arch is obtained with therecognized. The main pulmonary artery is more beam aligned from anterior right of the fetal chest toanterior and to the left of the other structures, and posterior left of the fetal chest (Table 7). In thetends to have a larger diameter. The ascending aorta ductal view, the main pulmonary artery, and ductalis the next, more rightward structure that is posi- arch are well seen and main pulmonary artery size istioned slightly posterior relative to the main pulmo- easily measured. The direction of ductal flow isnary artery. The superior vena cava is the most appreciated and the velocity recorded. Sweeping toposterior and rightward vessel of the 3. Slight dis- either side may allow visualization of the branchcrepancies in the position or size of these 3 vessels pulmonary arteries. As the ductus connects with thecan identify subtle pathology of the outlets and descending aorta, the isthmus is well seen and thearches. Anterior to the 3 vessels is the thymus, direction of flow established.21 In the aortic archwhich wraps over the anterior aspect of the superior view, antegrade flow though the ascending aorta,mediastinum. transverse arch, and descending aorta is established Cardiac long-axis view. The long-axis view is with color Doppler interrogation.aligned with the left ventricular outflow tract (Table Heart rate and rhythm. The rate and mechanism5). The continuity between the mitral and aortic of rhythm is established by identifying mechanicalvalves and the absence of sub-aortic conus is noted. events associated with both atrial and ventricularThe size of the ascending aorta is measured. Sweep- systole. Atrial systole is identified with either an
Journal of the American Society of EchocardiographyVolume 17 Number 7 Pediatric Council of the American Society of Echocardiography 809M-mode of the lateral atrial wall or atrial append- maximum temperature increase that may result fromage,22 pulse Doppler interrogation of the outflow the exposure at those ultrasound system settings istract at a location where atrioventricular valve in- 2°C). The risk of mechanically induced ultrasoundflow is detected,23 or pulse tissue Doppler of the damage is displayed by the mechanical index (MI),atrial wall.14 The identification of atrioventricular which is defined as the ratio of maximal peakvalve inflow serves as a proxy for atrial systole. rarefractional pressure to the square root of theVentricular systole can be identified with M-mode of ultrasound frequency. The risk of mechanical injurythe ventricular free wall or aortic valve or again, rises with increasing MI.using pulse Doppler interrogation of the outflow As newer modalities such as Doppler applicationstract or tissue Doppler of the ventricular myocar- assessing tissue motion and real-time 3-dimensionaldium. Doppler flow in the outflow tract serves as a imaging continue to develop, bioeffects on the fetusproxy for ventricular systole. Measurement of the will need to continue to be monitored. As there aretime interval between two successive beats allows no strictly defined limits established, use of ultra-calculation of rate. Simultaneous interrogation of left sound energy in fetal echocardiography is bestventricular inflow and outflow allows assessment of expressed by the “ALARA” principle—as low asatrioventricular conduction and the “mechanical” reasonably achievable.28PR interval.23 SUMMARYULTRASOUND SAFETY DURING PREGNANCY The fetal echocardiogram is a unique ultrasound examination, which differs from the antenatal ob-The standard fetal echocardiographic examination stetrical ultrasound and from the conventional echo-utilizes all modalities of diagnostic ultrasound in- cardiogram in the infant, child, or adult. A unique,cluding 2-dimensional (B-mode) imaging, Doppler, high level set of skills and knowledge is required inand Doppler color flow mapping. Ultrasound energy order to perform this test. In this statement, weexpenditures increase with each modality used and outline the indications and essential performanceare most intense when Doppler color flow mapping components of the fetal echocardiogram, as well asis applied to a small region of interest, as is com- highlight the importance of operator cognizance ofmonly the case when examining the structures of potential safety concerns. This statement contrib-the fetal heart.24 Hence special consideration should utes to the establishment of a standard for perfor-be given to the use of ultrasound energy in the mance of the fetal echocardiogram, as the use of thisdeveloping fetus. While theoretical concerns exist, valuable assay continues to expand in the future.to date there have been no confirmed harmfuleffects detected.25 Those performing fetal echocar- We wish to acknowledge Dr David Low for his artisticdiography should be aware of these effects and contributions to this report.should limit power output and time of exposure tono more than that which is absolutely necessary tocomplete the examination. As ultrasound technology has advanced and new REFERENCESmodalities added, power output on newer systemshas changed. In 1985, the Food and Drug Adminis- 1. Hoffman JI, Kaplan S. The incidence of congenital hearttration 510(K) guide strictly limited ultrasound disease. J Am Coll Cardiol 2002;39:1890-900. 2. Verheijen PM, Lisowski LA, Stoutenbeek P, Hitchcock JF,power output on imaging systems. However, since Brenner JI, Cope JA, et al. 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